Host-feeding preferences of Culex pipiens and its potential significance for flavivirus transmission in the Camargue, France

Abstract

The spread of the West Nile (WNV) and Usutu (USUV) flaviviruses in Europe in recent decades highlights the urgent need to understand the transmission networks of these pathogens as a basis for effective decision-making. These viruses are part of a complex disease cycle that involves birds as principal hosts and humans and horses as dead-end hosts. Our study aims to uncover the intricate relationships between the main mosquito vector of these viruses, Culex pipiens L. (Diptera: Culicidae) and its feeding preferences based on the forage ratio among several host species, primarily birds in a land-use gradient. We estimated the bird host potential to act as a host for flavivirus, the reservoir capacity index, based on forage ratios and potential host competence based on molecular prevalence. We sampled mosquitoes and, at the same time, conducted bird censuses in the Camargue region in southern France, where co-circulation of these viruses has been reported. Several localities were sampled along a land-use gradient in peri-urban, agricultural and natural areas from May to November 2021. We identified 55 vertebrate species in 110 engorged Cx. pipiens by PCR amplification and sequencing of mitochondrial 12S and 16S Ribosomal DNA genes. Culex pipiens feeds primarily on 51 bird species and secondarily on two mammals, one amphibian and one reptile. Based on forage ratios, we found a preference of Cx. pipiens in the Camargue for the order Passeriformes and, more specifically, for Columba livia domestica L. (Columbiformes: Columbidae) in agricultural areas, and for Passer domesticus/montanus L. (Passeriformes: Passeridae), in agricultural and peri-urban areas. The natural habitats had significantly higher forage ratio values than agricultural and peri-urban areas. We suggest that certain key species, such as Passer sp., Columba livia and Turdus sp., might be potentially considered locally relevant hosts for transmission in this area, as they are important for mosquito feeding and also potentially important hosts for flavivirus amplification. These data will be beneficial in understanding host-vector interactions and the relationships between bird communities, mosquito feeding preferences and emerging mosquito-borne diseases.

Keywords: Camargue; Culex pipiens; France; Usutu; West Nile virus; bloodmeal preferences; forage ratio; mosquito‐borne diseases.

FIGURE 1

Map showing the three study areas in the Camargue region with their land‐use classifications. Each study area incorporates the three land‐use types (habitats), each of which encompasses different types of land cover: peri‐urban (black triangles; artificial surfaces), agricultural (black diamonds; agricultural areas) and natural (black dots; wetlands and forests).

FIGURE 2

Average forage ratio (selectivity index) of Culex pipiens for the vertebrate families (left panel: a) and the principal host species (right panel: b) compared with the mean host abundance. The forage ratio values are represented on the right side of the y‐axis; the higher the value, the greater the selectivity of Cx. pipiens for the host. The values on the left side of the y‐axis represent the mean abundances of each bird family (panel a) and each host species (panel b).

FIGURE 3

Host preferences based on Culex pipiens forage ratios. Results for the principal bird species in the different habitats: peri‐urban, agricultural and natural.

FIGURE 4

Relationship among habitat and bird richness (left panel), and habitat and forage ratio (right panel). These differences among habitats are statistically significant (Table 2).

FIGURE 5

West Nile virus (WNV) reservoir capacity index for the main bird species. We multiplied the forage ratio by the estimated host competence of each bird species for WNV based on molecular prevalence (Tolsá‐García et al., 2018), and we divided by 100 to calculate a percentage.